Promoter Islands in the Genome of \emph{E. coli}: Comparative Analysis against AT-Rich Sequences

O. A. Glazunova ; S. S. Kiselev ; K. S. Shavkunov ; A. A. Bykov ; V. V. Panyukov ; O. N. Ozoline

Matematičeskaâ biologiâ i bioinformatika, Tome 9 (2014) no. 2, pp. 563-574.

Résumé

The functional properties of E. coli genome promoter islands, which are special regions with abnormally high contents of transcription signals, are compared to those of genomic areas, which are unusually rich in A/T-pairs. It was shown that computational sets of regions for both types partially overlap by certain criteria, while their functional properties are much alike. At the same time, promoter islands are characterized by a higher potential for synthesis of short oligonucleotides, as compared to AT-rich sequences. Such RNAs may be the target products of these unusual sites or byproducts of their suppressed state. The islands are richer in inverted repeats than AT-rich regions, and much richer compared with regular promoters. Considering that such structural elements commonly serve as targets for interactions with dimer or tetramer forms of regulatory proteins, it can be assumed that transcription initiation from island-embedded promoters is under control of the regulatory network of cells. Thus, the resulting RNA products might be required for normal cell functioning. This idea is also supported by experimentally confirmed high yield of oligonucleotide product from the island promoter inside the yjgL.

Bibliographie

[1] Shavkunov K. S., Masulis I. S., Tutukina M. N., Deev A. A., Ozoline O. N., “Gains and unexpected lessons from genome-scale promoter mapping”, Nucl. Acids Res., 37 (2009), 4919–4931 | DOI

[2] Panyukov V. V., Ozoline O. N., “Promoters of Escherichia coli versus promoter islands: function and structure comparison”, PLoS ONE, 8 (2013), e62601 | DOI

[3] Panyukov V. V., Kiselev S. S., Shavkunov K. S., Masulis I. S., Ozoline O. N., “Mixed promoter islands as genomic regions with specific structural and functional properties”, Mathematical Biology and Bioinformatics, 8 (2013), t12–t26

[4] Shavkunov K. S., Tutukina M. N., Masulis I. S., Ozoline O. N., “Promoter islands: the novel elements in bacterial genomes”, J. Biomol. Struct. Dyn., 28 (2011), 1128–1129

[5] Syvanen M., “Evolutionary implications of horizontal gene transfer”, Annu. Rev. Genet., 46 (2012), 341–358 | DOI

[6] Lucchini S., Rowley G., Goldberg M. D., Hurd D., Harrison M., Hinton J. C., “H-NS mediates the silencing of laterally acquired genes in bacteria”, PLoS Pathog., 2 (2006), e81 | DOI

[7] Navarre W. W., Porwollik S., Wang Y., McClelland M., Rosen H., Libby S. J., Fang F. C., “Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella”, Science, 313 (2006), 236–238 | DOI

[8] Dorman C. J., “Horizontally acquired homologues of the nucleoid-associated protein H-NS: implications for gene regulation”, Mol. Microbiol., 75 (2010), 264–267 | DOI

[9] Dorman C. J., Genome architecture and global gene regulation in bacteria: making progress towards a unified model?, Nat. Rev. Microbiol., 11 (2013), 349–355 | DOI

[10] Dorman C. J., “H-NS-like nucleoid-associated proteins, mobile genetic elements and horizontal gene transfer in bacteria”, Plasmid., 75 (2014), 1–11 | DOI

[11] Salgado H., Peralta-Gil M., Gama-Castro S., Santos-Zavaleta A., Muñiz-Rascado L., García-Sotelo J. S., Weiss V., Solano-Lira H., Martínez-Flores I., Medina-Rivera A., Salgado-Osorio G., Alquicira-Hernández S., Alquicira-Hernández K., López-Fuentes A., Porrón-Sotelo L., Huerta A. M., Bonavides-Martínez C., Balderas-Martínez Y. I., Pannier L., Olvera M., Labastida A., Jiménez-Jacinto V., Vega-Alvarado L., Del Moral-Chávez V., Hernández-Alvarez A., Morett E., Collado-Vides J., “RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more”, Nucl. Acids Res., 41 (2013), D203–D213 | DOI

[12] Panyukov V. V., Nazipova N. N., Ozolin O. N., “Paket programm aSHAPE dlya izucheniya prostranstvennoi konformatsii uchastkov bakterialnogo genoma”, Matematicheskaya biologiya i bioinformatika, 6 (2011), 211–227

[13] Okonechnikov K., Golosova O., Fursov M., the UGENE team, “Unipro UGENE: a unified bioinformatics toolkit”, Bioinformatics, 28 (2012), 1166–1167 | DOI

[14] Reppas N. B., Wade J. T., Church G. M., Struhl K., “The transition between transcriptional initiation and elongation in E. coli is highly variable and often rate limiting”, Mol. Cell., 24 (2006), 747–757 | DOI

[15] Kahramanoglou C., Seshasayee A. S. N., Prieto A. I., Ibberson D., Schmidt S., Zimmermann J., Benes V., Fraser G. M., Luscombe N. M., “Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli”, Nucl. Acids Res., 39 (2011), 2073–2091 | DOI

[16] Dornenburg J. E., DeVita A. M., Palumbo M. J., Wade J. T., “Widespread antisense transcription in Escherichia coli”, mBio, 1 (2010), e00024-10 | DOI

[17] Lawrence J. G., Ochman H., “Molecular archaeology of the Escherichia coli genome”, Proc. Natl. Acad. Sci. USA, 95 (1998), 9413–9417 | DOI

[18] Nakamura Y., Itoh T., Matsuda H., Gojobori T., “Biased biological functions of horizontally transferred genes in prokaryotic genomes”, Nat. Genet., 36 (2004), 760–766 | DOI

[19] Price M. N., Dehal P. S., Arkin A. P., “Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli”, Genome Biol., 9 (2008), R4 | DOI

[20] Huang Q., Cheng X., Cheung M. K., Kiselev S. S., Ozoline O. N., Kwan H. S., “High-density transcriptional initiation signals underline genomic islands in bacteria”, PLoS ONE, 7 (2012), e33759 | DOI

[21] Langille M. G., Brinkman F. S., “IslandViewer: an integrated interface for computational identification and visualization of genomic islands”, Bioinformatics, 25 (2009), 664–665 | DOI

[22] Ozoline O. N., Deev A. A., “Predicting antisense RNAs in the genomes of Escherichia coli and Salmonella typhimurium using promoter-search algorithm PlatProm”, J. Bioinf. Comput. Biol., 4 (2006), 443–454 | DOI

[23] Kiselev S. S., Ozoline O. N., “Structure-specific modules as indicators of promoter DNA in bacterial genomes”, Mathematical Biology and Bioinformatics, 6 (2011), t1–t13

[24] Oshima T., Ishikawa S., Kurokawa K., Aiba H., Ogasawara N., “Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase”, DNA Res., 13 (2006), 141–153 | DOI

[25] Dorman C. J., “H-NS, the genome sentinel”, Nat. Rev. Microbiol., 5 (2007), 157–161 | DOI